Aberrant functional connectivity between reward and inhibitory control networks in pre-adolescent binge eating disorder

Abstract

Background Behavioral features of binge eating disorder (BED) suggest abnormalities in reward and inhibitory control. Studies of adult populations suggest functional abnormalities in reward and inhibitory control networks. Despite behavioral markers often developing in children, the neurobiology of pediatric BED remains unstudied. Methods 58 pre-adolescent children (aged 9–10-years) with BED (mBMI = 25.05; s.d. = 5.40) and 66 age, BMI and developmentally matched control children (mBMI = 25.78; s.d. = 0.33) were extracted from the 3.0 baseline (Year 0) release of the Adolescent Brain Cognitive Development (ABCD) Study. We investigated group differences in resting-state functional MRI functional connectivity (FC) within and between reward and inhibitory control networks. A seed-based approach was employed to assess nodes in the reward [orbitofrontal cortex (OFC), nucleus accumbens, amygdala] and inhibitory control [dorsolateral prefrontal cortex, anterior cingulate cortex (ACC)] networks via hypothesis-driven seed-to-seed analyses, and secondary seed-to-voxel analyses. Results Findings revealed reduced FC between the dlPFC and amygdala, and between the ACC and OFC in pre-adolescent children with BED, relative to controls. These findings indicating aberrant connectivity between nodes of inhibitory control and reward networks were corroborated by the whole-brain FC analyses. Conclusions Early-onset BED may be characterized by diffuse abnormalities in the functional synergy between reward and cognitive control networks, without perturbations within reward and inhibitory control networks, respectively. The decreased capacity to regulate a reward-driven pursuit of hedonic foods, which is characteristic of BED, may in part, rest on this dysconnectivity between reward and inhibitory control networks.

Sex differences in regional gray matter density in pre-adolescent binge eating disorder: a voxel-based morphometry study

“…While both estrogen and progesterone – which has an antagonistic effect on estrogen – are elevated in those with BED, these findings pose the intriguing question around whether the sex hormones linked to greater binge eating are also linked to altered synaptic pruning and gray matter arborization. While altered synaptic pruning and arborization would impact the functional connectivity between gray matter structures, recent evidence has illustrated pervasive functional dysconnectivity in pre-adolescent children with BED (Murray et al, 2022a), which persists into adulthood (Haynos et al, 2021). However, the delineation of potential sex differences in functional connectivity would be critical in advancing this line of inquiry.…”

“…This is especially salient to examine in pre-adolescent and adolescent populations, where the prevalence of BED gradually shifts from a relatively even distribution between sexes, to a post-pubertal skew in prevalence towards females (Mikhail et al, 2021). To that end, assessing GMD may be an important starting point in this line of inquiry, given (i) the differential rates of gray matter development in boys and girls throughout adolescence, respectively (Gennatas et al, 2017), and (ii) evidence noting perturbations in GMD among children with BED, relative to controls (Murray et al, 2022a(Murray et al, , 2022b(Murray et al, , 2022c. However, given that gray matter morphometric changes evolve rapidly throughout adolescence, and in differential trajectories among boys and girls (Gennatas et al, 2017), the need to map neurodevelopmental changes throughout adolescence ought to be underscored.…”

“…In concert, tasks of inhibitory control are characterized by hypoactivity in regions implicated in the inhibitory control network among those with BED, such as the dorsolateral prefrontal cortex (dlPFC) and inferior frontal gyrus (IFG) (Balodis et al, 2013). Moreover, resting state activity among those with BED suggests a diffuse functional dysconnectivity between nodes of reward and inhibitory controls circuits in both adults and children (Haynos et al, 2021; Murray et al, 2022a). Studies assessing cortical and subcortical structural characteristics of BED are relatively sparse.…”

“…The present study therefore aimed to elucidate sex differences in cortical and subcortical gray matter characteristics associated with BED among pre-adolescent boys and girls, where disease prevalence is most comparably distributed across genders. In addition, we aimed to examine the relationship between one region of brain which reliably demonstrates structural (Murray et al, 2022b) and functional (Murray et al, 2022a) abnormalities in children with BED - the dlPFC, and mechanisms purportedly underpinning BED psychopathology – behavioral approach and inhibition. Specifically, we leveraged the Adolescent Brain Cognitive Development (ABCD) Study (Casey et al, 2018) to undertake the first known assessment of sex differences in GMD in pre-adolescent children with DSM-5 diagnosed BED.…”

The neurobiological reward system and binge eating: A critical systematic review of neuroimaging studies

“…Of these studies, there were five (83%) that used a seedbased approach and one (17%) that used a graph theory-based approach. Their results showed a higher connectivity between the different regions of the striatum in patients with BN, a lower connectivity between the frontal cortex and striatum in patients with BN and BED, as well as a lower connectivity between the different regions of the frontal cortex in patients with BN and BED (Canna et al, 2017;Haynos et al, 2021;Murray, Alba, et al, 2022;Wang et al, 2017;Wang et al, 2019). A lower frontostriatal connectivity was also related to a higher BE frequency (Haynos et al, 2021).…”